Keep your cool: Overwintering physiology in response to urbanization in the acorn ant, Temnothorax curvispinosus.

Winter presents a challenge for survival, yet temperate ectotherms have remarkable physiological adaptations to cope with low-temperature conditions. Under recent climate change, rather than strictly relaxing pressure on overwintering survival, warmer winters can instead disrupt these low-temperature trait-environment associations, with negative consequences for populations. While there is increasing evidence of physiological adaptation to contemporary warming during the growing season, the effects of winter warming on physiological traits are less clear. To address this knowledge gap, we performed a common garden experiment using relatively warm-adapted versus cold-adapted populations of the acorn ant, Temnothorax curvispinosus, sampled across an urban heat island gradient, to explore the effects of winter conditions on plasticity and evolution of physiological traits. We found no evidence of evolutionary divergence in chill coma recovery nor in metabolic rate at either of two test temperatures (4 and 10 °C). Although we found the expected plastic response of increased metabolic rate under the 10 °C acute test temperature as compared with the 4 °C test temperature, this plastic response, (i.e., the acute thermal sensitivity of metabolic rate), was not different across populations. Surprisingly, we found that winter-acclimated urban ant populations exhibited higher heat tolerance compared with rural ant populations, and that the magnitude of divergence was comparable to that observed among growing-season acclimated ants. Finally, we found no evidence of differences between populations with respect to changes in colony size from the beginning to the end of the overwintering experiment. Together, these findings indicate that despite the evolution of higher heat tolerance that is often accompanied by losses in low-temperature tolerance, urban acorn ants have retained several components of low-temperature physiological performance when assessed under ecologically relevant overwintering conditions. Our study suggests the importance of measuring physiological traits under seasonally-relevant conditions to understand the causes and consequences of evolutionary responses to contemporary warming.

Adaptation to Urban Heat Islands Enhances Thermal Performance Following Development under Chronic Thermal Stress but Not Benign Conditions in the Terrestrial Isopod Oniscus asellus.

AbstractThe effects of chronic thermal stress during development on thermal performance traits are not well characterized under urban heat islands, despite these conditions being biologically relevant for how organisms experience the urban environment and the often strong linkages between thermal performance traits and fitness. Here we use the terrestrial isopod Oniscus asellus to examine the effects of chronic thermal stress during development on voluntary running speed of urban and rural isopods. We used a laboratory common-garden experiment design with two developmental acclimation temperature treatments (21°C, a benign treatment, and 29°C, a stressful treatment) and three test temperatures (19°C, 31°C, 40°C); we tested running speed of individuals from urban and rural populations under each of the temperature combinations. We found that for both urban and rural isopods, running speed across three test temperatures was reduced under developmental acclimation conditions of 29°C compared with 21°C. Importantly, however, urban isopods had a running speed advantage over the rural isopods under the 29°C developmental acclimation conditions at the lower two test temperatures. No population differences were detected under benign developmental acclimation conditions of 21°C. The evolution of higher heat tolerance in urban isopods further supported the interpretation of adaptation to heat stress. Convergence of urban and rural isopod running speed at the highest test temperature, however, suggests potential limits or constraints on adaptation. Our results indicate that thermal adaptation to urban heat islands can mitigate negative effects of chronic developmental thermal stress, even when overall performance is reduced compared with benign conditions.

Evidence for the evolution of thermal tolerance, but not desiccation tolerance, in response to hotter, drier city conditions in a cosmopolitan, terrestrial isopod.

Cities are often hotter and drier compared with nearby undeveloped areas, but how organisms respond to these multifarious stressors associated with urban heat islands is largely unknown. Terrestrial isopods are especially susceptible to temperature and aridity stress as they have retained highly permeable gills from their aquatic ancestors. We performed a two temperature common garden experiment with urban and rural populations of the terrestrial isopod, Oniscus asellus, to uncover evidence for plastic and evolutionary responses to urban heat islands. We focused on physiological tolerance traits including tolerance of heat, cold, and desiccation. We also examined body size responses to urban heat islands, as size can modulate physiological tolerances. We found that different mechanisms underlie responses to urban heat islands. While evidence suggests urban isopods may have evolved higher heat tolerance, urban and rural isopods had statistically indistinguishable cold and desiccation tolerances. In both populations, plasticity to warmer rearing temperature diminished cold tolerance. Although field-collected urban and rural isopods were the same size, rearing temperature positively affected body size. Finally, larger size improved desiccation tolerance, which itself was influenced by rearing temperature. Our study demonstrates how multifarious changes associated with urban heat islands will not necessarily contribute to contemporary evolution in each of the corresponding physiological traits.

Remarkable insensitivity of acorn ant morphology to temperature decouples the evolution of physiological tolerance from body size under urban heat islands.

Environmental temperature can alter body size and thermal tolerance, yet the effects of temperature rise on the size-tolerance relationship remain unclear. Terrestrial ectotherms with larger body sizes typically exhibit greater tolerance of high (and low) temperatures. However, while warming tends to increase tolerance of high temperatures through phenotypic plasticity and evolutionary change, warming tends to decrease body size through these mechanisms and thus might indirectly contribute to worse tolerance of high temperatures. These contrasting effects of warming on body size, thermal tolerance, and their relationship are increasingly important in light of global climate change. Here, we used replicated urban heat islands to explore the size-tolerance relationship in response to warming. We performed a common garden experiment with a small acorn-dwelling ant species collected from urban and rural populations across three different cities and reared under five laboratory rearing temperatures from 21 to 29 °C. We found that acorn ant body size was remarkably insensitive to laboratory rearing temperature (ant workers exhibited no phenotypic plasticity in body size across rearing temperature) and among populations experiencing cooler rural versus warmer urban environmental temperatures (no evolved differences in body size between urban and rural populations). Further, this insensitivity of body size to temperature was highly consistent across each of the three cities we examined. Because body size was robust to temperature variation, previously described plastic and evolved shifts in heat (and cold) tolerance in acorn ant responses to urbanization were shown to be independent of shifts in body size. Indeed, genetic (colony-level) correlations between heat and cold tolerance traits and body size revealed no significant association between size and tolerance. Our results show how typical trait correlations, such as between size and thermal tolerance, might be decoupled as populations respond to contemporary environmental change.

Evolution, not transgenerational plasticity, explains the adaptive divergence of acorn ant thermal tolerance across an urban-rural temperature cline.

Although studies increasingly disentangle phenotypic plasticity from evolutionary responses to environmental change, few test for transgenerational plasticity in this context. Here, we evaluate whether phenotypic divergence of acorn ants in response to urbanization is driven by transgenerational plasticity rather than evolution. F2 generation worker ants (offspring of laboratory-born queens) exhibited similar divergence among urban and rural populations as field-born worker ants, suggesting that evolutionary divergence rather than transgenerational plasticity was primarily responsible for shifts toward higher heat tolerance and diminished cold tolerance in urban acorn ants. Hybrid offspring from matings between urban and rural populations also indicated that evolutionary divergence was likely the primary mechanism underlying population differences in thermal tolerance. Specifically, thermal tolerance traits were not inherited either maternally or paternally in the hybrid pairings as would be expected for strong parental or grandparental effects mediated through a single sex. Urban-rural hybrid offspring provided further insight into the genetic architecture of thermal adaptation. Heat tolerance of hybrids more resembled the urban-urban pure type, whereas cold tolerance of hybrids more resembled the rural-rural pure type. As a consequence, thermal tolerance traits in this system appear to be influenced by dominance rather than being purely additive traits, and heat and cold tolerance might be determined by separate genes. Though transgenerational plasticity does not appear to explain divergence of acorn ant thermal tolerance, its role in divergence of other traits and across other urbanization gradients merits further study.

The role of tolerance variation in vulnerability forecasting of insects.

Quantifying the amount of climatic change organisms can withstand before exceeding their physiological tolerance is a cornerstone of vulnerability forecasting. Yet most work in this area treats tolerance as a fixed trait. We review recent work that quantifies variation in high temperature tolerance across bioclimatic gradients, and we explore the implications for vulnerability to climate change. For some sources of variation, including differences in the evolutionary potential of heat tolerance across latitude, the typical biogeographic pattern of high vulnerability in the tropics is exacerbated. For other sources of variation, including certain types of plastic variation in heat tolerance, the biogeographic pattern of high tropical vulnerability is diminished. As a consequence, thermal tolerance variation should not be ignored in vulnerability forecasting.